Monday, April 28, 2014

In view of the Mallard: on ecological fitting and non-fitting

Collecting things (coins, stamps, music, guitars, cars) is the nature of humans (and Bowerbirds), and I am not immune to it. My single-malt Whisky collection is up around 50 different bottles, although it is different from most collections in that it suffers constant turnover. One particular type of collecting – I am sure there is an official name for it that I don’t know – occurs when traveling: one purchases the same item with only a minor change (usually the name of the place) everywhere one goes. How about that cupboard full of otherwise identical Starbuck’s mugs from London, New York, San Francisco, and a host of other cities? And you simply must get that new one I heard of – from Greenland! A collection of this sort tells the visitor to your house that I went to all these cool places and I want you to know it but I don’t have to tell you because you can see it in front of you. In essence, you are collecting and displaying places rather than things.

Stockholm – prime Mallard habitat, but then where isn’t?
I found a particularly puzzling version of this phenomenon in the back recesses of an out-of-the-way cupboard when we moved into our new house some years ago. It was in several big Mason jars and closer examination revealed hundreds of matchbooks, each with a different restaurant or hotel imprinted on it. These are the kinds of collections that detectives in Hollywood movies use to track down the whereabouts of some otherwise cryptic serial killer. I have to confess, however, that I haven’t spent much time reading the actual business names on the matchbooks, and their presence in the jars has steadily dwindled to a fraction of its former exuberance. (It is a lot easier to just go back to the jar than it is to remember where I put those damn matches I got out yesterday.)

I don’t suffer from this habit of collecting while traveling – except for pictures of wildlife. The trouble with wildlife pictures in the above context is that they aren’t of the same thing with some small indication that they come from a different place (like those Starbuck's mugs). They instead show huge turnover from place to place. Just a few days ago, however, I was in Stockholm walking around in the beautiful spring weather and trying to find wildlife to photograph when I saw a Mallard.

The Stockholm Mallard that started it all.
Everywhere I travel I see Mallards and I rarely take a picture as they are so boring and ubiquitous. In fact, I only take a picture of a Mallard when they are the only thing to take a picture of; and when taking the picture, I always think to myself: Why the hell am I taking a picture of this Mallard? I will never do anything with the photo anyway! But then it struck me: Mallards can be my match books, my Starbuck’s mugs, my t-shirts, my hats. I can take pictures of Mallards everywhere I go – well over half the world, anyway.

The current distribution of Mallards. They were introduced to Australia and New Zealand and presumably will eventually cover the globe.
In my dotage, I can display all my Mallard pictures in one of those picture frames designed for multiple small pictures – or maybe one of those electronic picture displays that sits on the table and cycles through photos. Right then and there, Mallards became a key goal of my future trips. Everywhere I go, I will be asking my surprised hosts: Can you please take me somewhere where I can see a Mallard? Now, no matter how urban, no matter how short the trip, I can have a good reason to bring my camera and take a walk looking for birds – a bird, that is.

The Stockholm Mallard again – or, wait, maybe it’s a different one.
By now you are probably thinking that the joke is on me, because Mallards look the same everywhere. What would be the point of taking a picture of them in each place – and surely nothing would come of displaying them? Or perhaps you are thinking that this is a type of place-collecting for which it is easy to cheat. You actually have to go to London to get a London Starbuck’s cup (or someone has to go for you) and a cup you buy in New York can’t be mistaken for one you bought in Stockholm. With Mallards, however, I could take a hundred photos of the same bird outside my house in Montreal, label each as coming from a different country and no one would know the difference. Or I could take the same Mallard (or maybe just a Mallard model) to every city and take a picture in front of ineffable landmarks (the Eiffel Tower, Times Square, the Sydney Opera House, and so on). It would be like that gnome that traveled the world in one my favorite movies, Amelie.

An Amsterdam Mallard fitting into a new frosty habitat.
Mulling over these thoughts in the bright sunshine, staring at a Mallard who was steadfastly ignoring my existence, brought me all the way back to 2001 when I was giving a job interview at the University of Pennsylvania. One of the first faculty members I met with after my talk was Dan Janzen. I didn’t know much of his work at the time but I did know he was famous, and so I resolved to pay attention – I was angling for a job after all. Remarkably he seemed not to have gotten the point of my talk as I imagined an astute naturalist would have done. My talk had been about rapid adaptive evolution (in only 14 generations) of trait differences between introduced salmon populations. How cool is that? Even Science thought it was cool enough to publish – something that hasn’t happened for me again in the subsequent 14 years. But all Dan wanted to talk about was how I should be more interested in why many organisms look the same in different places. Coyotes are pretty much the same from northern Alaska to Panama, Great Blue Herons from Alaska to Galapagos, Great White sharks from Newfoundland to Cape Town, and so on. Hmm, I said, hoping to seem intelligent.

A Montreal Mallard. At least I think that is where this was taken, as I didn’t think to label it – who would bother? It was only a Mallard.
Perhaps he could tell I was unconvinced, or perhaps he just wanted to increase his citations, because he then handed me a paper he had written. It was a short opinion piece (sort of a blog post, before blogs existed) about “ecological fitting,” in which he explained the phenomenon and gave its name. In essence, organisms find ways to retain their existing way of life in a new environment, which reduces selection on them and allows/requires them to stay much the same. (Gene flow is another reason why organisms might be very similar across large ranges, an idea pushed most recently by Doug Futuyma in his hypothesis of “ephemeral divergence.”)

Another Stockholm Mallard – this one looks a bit different for some reason.
I hadn’t thought too much about ecological fitting in the 13 years between then and now, but it all came back in a rush staring at the damn Mallard and thinking about the implications of my new world-wide photo-collecting quest. Surely Mallards were the best example of ecological fitting in existence – they look and act bloody well the same across their huge distribution. Why might this be so? Without bothering to read any literature that might exist on the topic (this is a blog, after all), I will speculate that ecological fitting will be most common for organisms that have key habitat needs that are similar everywhere (Mallards need shallow water – found worldwide) and diets that are independent of particular prey species (Mallards eat aquatic plants of many sorts – at least I imagine they do). The same is true of Great Blue Herons (they eat any type of small fish) and coyotes (they pretty much eat anything) and great white sharks and so on.

Some Mallards in California – or maybe Edmonton. I can't remember.
Then, for just a moment, I thought about it from the Mallard’s perspective looking back at me. What would a well-traveled Mallard with a camera (maybe a GoPro with unlimited batteries strapped to its head) experience in an effort to collect photographs of humans, which are also distributed worldwide? I am pretty sure he wouldn’t come up with the idea of ecological fitting (even if he weren’t a duck) because humans are hugely variable from place to place, most obviously in color and stature. In fact, this effect was staring me in the face: Swedes are HUGE. When I travel to the tropics of South America, I am nearly always the tallest person in a crowd – except for the occasional person from higher latitudes – but when in Sweden, I am average or a bit below. This non-constancy of humans (in comparison to Mallards anyway) was quite literally staring me in the face. Still mulling this over in my head as the duck swam off (to be replaced by another that looked pretty much the same), I realized that I had already explored this non-constancy in my own research. 

Some Kelowna (British Columbia) Mallards. (Yes, I realize it is a female, but you know what the male looks like.)
I used to live across a small canal from a biking/walking path. In the summers, I would sit outside in the warm sun and play with the kids or read a book or mow the lawn or whatever. In doing so, I would be in view of a constant stream of humans walking by on the path in front of me – and they seemed immensely variable. This apparent variation got me to wondering: are humans more variable than other organisms, as they seemed in that moment? To answer the question, I recruited a Master’s student , Ann McKellar. We (when I say “I” I mean “we” and when I say “we” I mean “she”) collated data from hundreds of human populations and hundreds of animal species for a trait that would be comparable among all of them – height/length. Analysis of these data showed that, contrary to my naive expectation from the lawn in my backyard, and more in line with the view of the Mallard, humans were about as variable among populations as were other animals (for example, they follow “Bergmann’s Rule” of being larger at higher latitudes – Swedes vs. Ecuadorians) but they were much less variable within populations than were other animals. We suggested in the paper that humans are the antithesis of “ecological fitting” (although we didn’t use that term) in that selection seems to have favored particular forms in particular places.

Some New Orleans Mallards. I realize the photo is crappy but I had to crop this out of the corner of a photo I took of a much cooler bird. No one ever intentionally takes pictures of Mallards when cooler birds are around.
Of course, everything is now changing. Humans from all over the world are migrating to all other places in the world (my neighbours are from Germany, Norway, Sweden, France, Italy, and even New Caledonia) and doing quite well in their new habitats – buffered by our technological solutions that make climate similar within houses from Ecuador to Alaska. Eventually, due to such migration, we might imagine that humans will be quite similar among locations but quite variable within them. This isn’t ecological fitting in the classic sense because humans won’t look the same everywhere, instead they will look different WITHIN everywhere. So we will need some new term (gotta love coining terms in blogs – "squib traits,” anyone? – where it has no real consequence for the literature) – perhaps “ecological ignorance,” although maybe that can have too many meanings. I am sure readers of this blog can come up with other, better, suggestions.

Some Laval (Quebec) Mallards in a snow storm. (They look like normal Mallards when the snow clears.)
In the meantime, I intend to continue my nascent photo collection of the World’s Mallards. So, if I happen to visit you in the years to come, please scope out a good Mallard sanctuary for me. I will bring my camera – and a Mallard model in case you can’t find me a real one.

More Mallards on the way.

Dan Janzen's paper: On Ecological Fitting

Doug Futuyma's paper on ephemeral divergence: Evolutionary Constraint and Ecological Consequences

Our paper on How Humans Differ from Other Animals in their Levels of Morphological Variation.


Mallards photographed since this post was first published:

New Orleans, LA, USA, Dec. 2014
Saskatoon, SK, Canada, May 2015

Napa, CA, USA, Dec. 2015
Sanssouci Park, Potsdam, Germany, June 2016.
Lago Maggiore, southern Switzerland, June 2016.

Wednesday, April 23, 2014

The Blog Québécoise: Niche Constructed Community Monopolization

Community monopolization. Evolutionary monopolization. Cultural Monopolization. In this post, I hope to weave these concepts together into a unified whole by means of an analogy based on Québec and its politics. 

The early bird gets the worm. This simple statement is the universal acknowledgement that, when resources are limited, the first individual to arrive at a given location will – all else being equal – obtain the most resources. This monopolization of resources by early individuals can sometimes be so strong as to prevent the establishment of later individuals. That is, early birds can exclude late birds – even if they are otherwise identical in their foraging ability.

These priority effects can extend beyond individuals. For instance, the idea of “community monopolization” posits that early-arriving species can monopolize resources and exclude late-arriving (but otherwise identical) species from a given location. Community assembly thus can be a simple function of the order in which species arrive, rather than their different traits or functional abilities. As an extreme example, species A might be better adapted than species B for a given location, but if species B gets there first, it can monopolize resources and exclude the otherwise superior species A. The same logic can apply to different types within a single species. That is, early-arriving phenotypes/genotypes might monopolize resources and exclude late-arriving phenotypes/genotypes – even if the late arrivers would otherwise be better adapted.

The early bird might also evolve to get the worm. Envision two functionally-equivalent species (or phenotypes/genotypes) that could colonize a new location, such as a new pond forming in a region with two different clones of the zooplankton Daphnia. Dispersal is limited across the landscape, and so the two clones are unlikely to arrive at the same time – perhaps one arrives several months before the other. In this case, the early-arriving clone could rapidly evolve adaptations that better suit them for the new environment (Daphnia can show rapid evolution within a single summer). When the second clone eventually arrives, it finds a now better-adapted clone already present and the second clone is therefore excluded. Evolutionary monopolization.

The Question: Image stolen from one of Luc De Meester's presentations.

All of this might be just academic speculation, except that the question is germane to changes in community structure as a result of climate change – with Daphnia providing a nice test case. Daphnia show adaptation to temperature, such that clones living in a warmer environment have higher fitness (survival and reproduction) in that environment than do Daphnia adapted to cold environments. Daphnia also move extensively across the landscape, such as when their resting eggs stick to a bird’s legs. So how will adaptation and dispersal interact to shape community assembly under climate warming? Perhaps northern cold-adapted populations will simply be replaced by migrants from southern populations that have a long history of adaptation to warm conditions. Alternatively, perhaps northern cold-adapted populations will rapidly adapt to the warming conditions, and thereby exclude the southern immigrants that would otherwise have been better suited for the new warmer conditions.

The Basic Experiment: Image stolen from one of Luc De Meester's presentations.

Wendy Van Doorslaer, Luc De Meester and colleagues tested these possibilities by placing cold-adapted Daphnia clones from the UK into unheated (colder) and heated (warmer) mesocosms. After allowing the Daphnia to evolve for 1.5 years, they competed the two types of UK clones (from the warm treatment and from the cold treatment) against warm-adapted French clones from France. Under warm test conditions, the French clones were trounced by the UK clones – but only the UK clones that had been adapting in the heated tanks. In short, a period of adaptation by the UK clones to warm conditions had a huge effect in maintaining their success in the face of invading French clones. Evolutionary monopolization made flesh.

More Experimental Details: Image stolen from one of Luc De Meester's presentations.

I was telling this story to my lab group because we had recently read a couple of papers that had discussed community and evolutionary monopolization. I described the French versus UK Daphnia results and pointed out that Luc likes to invoke the 1000 years of French–UK human conflict as a way of adding humor to this French–UK Daphnia death match. At precisely this time, Québec was in the throes of a contentious election, pitting the incumbent Québec separatist party – the Parti Québécoise – against the opposition federalist Québec Liberal Party. This context means that the constant tension (or at least discussion) of Francophone vs. Anglophone issues in Québec was firmly in our minds – and we couldn’t help but start to wonder if Québec provided a useful (or at least fun and topical) analogy.
Québec was first colonized by the French, who then had 150 years largely to themselves (apart from First Nations peoples, who were greatly reduced by disease) before being conquered by the British. The British then did as much as they could – both subtly and not-so-subtly – to subjugate, assimilate, and control the French. At that point, French immigration to Canada greatly decreased and British immigration took off. As a result, most of Canada to the west of Québec is English speaking. Québec, however, retained its dominant French character – perhaps, as I will argue here, because they arrived first and built up a substantial population (55,000+) before the conquest, a critical mass that favored community monopolization and resisted British immigration.

The Key Result: Image stolen from one of Luc De Meester's presentations.

As time went on, however, the British population in Canada dramatically increased. The coincident increase in British immigration into Québec (from the rest of Canada) eventually started to overwhelm the French population (a similar effect – higher immigration can overcome the priority effect – is seen in the Daphnia experiments). Before the French population became a minority, however, they elected a series of governments that brought in language laws favorable to the French: Immigrants from Canada must send their kids to French school (Québec residents also must do so). Outside advertising has to be in French (including business names – KFC becomes Poulet Frit Kentucky). And so on. This created a new form of monopolization: cultural monopolization.

Translation = KFC. Image Source.

In cultural monopolization (I just made this term up, although it seems likely to already exist), governments and other societal institutions enact rules, regulations, and norms that favor the local populace over immigrants. And it seems to have worked in Québec. In a relatively short time, many English businesses left Québec and the proportion of Anglophones (and Allophones) stopped increasing. The result was a “niche constructed” cultural version of evolutionary monopolization, where local conditions are altered through time to be favorable to the local population and unfavorable to foreign immigrants.

If cultural monopolization – primarily through language – has been important in Québec, one would expect immigrants from similar environments (French-speaking countries) to be more successful than immigrants from different environments (non-French-speaking countries). Moreover, because French immigrants do not (as strongly) dilute the culture Québec is trying to protect, you would expect government policies to favor French immigrants over English immigrants, which is indeed the case. Immigration into Québec, which has its own immigration offices, is easier from French-speaking countries. Moreover, French students pay resident rather than foreign tuition. (Remarkably, French students pay lower tuition than non-Québec Canadian students.)

Of course, all of this effort to retain a French character in Québec might be for naught if the French residents commonly interbred with English immigrants – leading to a genetic and cultural mishmash that would dilute the “pure” Québec culture. Unless, of course, inter-breeding (hybridization?) was rare, with Francophone women (and men) preferring Francophone men (and women). Although I have no stats on this, a quick poll of our lab group indicated that people felt cultural (language) differences did actually lead to positive assortative mating – mixed Francophone-Anglophone pairings were much rarer that would be expected at random. The agreed exception was late in the evening at nightclubs when people didn’t really pay that much attention to what the other sex was saying anyway. Beer goggles become beer earplugs. However, late-night trysts that start in nightclubs probably rarely lead to immediate children and so, perhaps, assortative child production (try bringing an Anglophone boyfriend home to a Francophone separatist father!) is stronger than assortative mating.

Of course, all this speculation is simply fun, but it is nevertheless interesting to think how culture might be another form of monopolization. Indeed, a number of studies have shown that immigrants in non-human animals can have lower fitness simply because of cultural differences, such as different song types in birds.

Parti Québécoise leader resigns in wake of election defeat. Source

Interestingly, results of the election described above suggest cultural monopolization might be weakening. The party in power (the Parti Québécoise) was pushing, as a major campaign promise, a bill (the Québec Charter) that would have placed severe restrictions on immigrant non-Québec cultural expression, especially religious symbols of non-Catholics. I am pleased to say, however, that this strategy did not play well to the Québec electorate. The Parti Québécoise went down to a resounding defeat at the hands of the more tolerant Québec liberals. Along the same lines, the Québec separatist party at the Canadian Federal level (the Bloc Québécoise) was soundly defeated – obliterated, really – by Québec voters in the last federal election. A cynic might say that immigration is again starting to overwhelm Québec culture and that we need more efforts at community (and cultural) monopolization. But I am not a cynic. I think the changing tide indicates that the Québec public have a growing confidence that their culture is strong and interesting and will now survive without needing additional institutional protections. Cultural monopolization has become coolness monopolization. That is why my kids are in French school and someday I expect to have to entertain Francophone boyfriends. Of course, they will have to be speaking English if they want to communicate with me – familial monopolization?

Planning familial monopolization?

This talk of kids growing up and having boyfriends is so depressing that I can’t help but revel in the great fun we had last week converting Easter Egg Hunting into Easter Egg Bouldering.

The Van Doorslaer et al. paper

Thanks to Gregor Rolshausen for the title of this post.

Tuesday, April 15, 2014

Pupfish on the adaptive landscape, or: How I learned to stop worrying and love the cable tie

[ This post is by Christopher Martin; I am just putting it up.  –B. ]

Like most evolutionary biologists, when I think of evolution I imagine rugged mountain landscapes, as Carl Zimmer eloquently introduced the concept of the adaptive landscape. Try to imagine a vast landscape connecting the phenotypes of all organisms where spatial location indicates a particular phenotype and the terrain – the height at any particular location – corresponds to the fitness of each individual phenotype (a Simpsonian landscape) or genotype (the original Wrightian landscape from 1932) along this space. The species we observe in the wild are expected to sit on the tops of fitness peaks, isolated by fitness valleys from neighboring fitness peaks corresponding to other species: alternative phenotypes capable of surviving and reproducing in the same environment. In reality, of course, this picture is even more complex: environments fluctuate, phenotype and genotype ‘surfaces’ are high-dimensional, fitness is frequency-dependent, many-to-one mapping is pervasive, and fitness may continue to increase indefinitely even on the tops of ‘peaks’; the adaptive landscape may resemble something more like the foaming surface of the ocean than a stable mountain range.

Nonetheless, the adaptive landscape is a powerful metaphor that pervades evolutionary thinking. But it is also an empirical quantity that can be measured in the wild. Since Lande and Arnold’s watershed insight that fitness landscapes can be estimated directly, there has grown an enormously successful research field measuring fitness in natural populations. There are now hundreds of studies measuring the strength and form of selection within natural populations in the wild. These have provided many novel insights about how selection acts in the short term, and have posed new paradoxes, such as why there is an abundance of disruptive selection despite our expectation that most species should sit on fitness peaks and thus experience stabilizing selection.

However, most of these studies measured selection within a population at one or two time periods. Few studies have repeatedly measured fitness within the same environment or across multiple environments. Fewer still have measured fitness landscapes across multiple species or for the intermediate phenotypes between species. Yet, this is exactly the data we need in order to understand past evolutionary trajectories and make predictions about the future. Our understanding of the larger-scale features of fitness landscapes – those peaks and valleys connecting multiple species that we all so vividly imagine – is still in its infancy.

Ideally, to increase our understanding of these large-scale features of the adaptive landscape, we need systems that are not only rapidly speciating and undergoing major morphological and ecological transitions, but that are also amenable to laboratory hybridization and transport in order to measure the fitness of intermediate hybrid phenotypes rarely observed in the wild.  A small, charismatic group of fishes named after puppy dogs (they love to beg for food and wag their tails) offer all of these features: Caribbean pupfishes! It is indeed possible to breed thousands of hybrid pupfishes in the laboratory in a month and then transport these offspring in your checked luggage back to the tropics to measure their fitness in the wild. This was my dissertation research project.

Figure 1. (a) Field enclosure on San Salvador Island. (b) Cable ties.

Within saline lakes on the tiny island of San Salvador in the Bahamas, two ecological specialists and a generalist pupfish have rapidly evolved from a generalist algae-eating common ancestor within the past 10,000 years. Importantly, these species are still in the process of speciating and adapting to novel ecological niches, so measuring the relevant environment driving adaptive radiation is still possible. Secondly, all three species live and breed within exactly the same benthic littoral habitat, which means that any differences among the species cannot be attributed to different habitats or allopatric isolation; rather, they result from the distinct niche environments that these species experience within the same habitat. Third, this young sympatric species flock has all the features of a classic adaptive radiation: (1) morphological diversification rates 50 times faster than background rates, (2) novel ecological niches, with one species specialized for tearing the scales off other pupfishes (Video 1) and another specialized for crushing hard-shelled prey with a unique nasal appendage, and (3) fitness experiments measuring hybrid growth and survival in field enclosures that demonstrate that multiple fitness peaks due to competition are driving adaptive radiation in the wild.


Video 1. Cyprinodon desquamator, the scale-eating pupfish, feeding on a euthanized generalist pupfish. Filmed at 2000 frames per second.  (You can also view the video at a larger size at

Interestingly, just a single empirical snapshot of the complex fitness landscape on this island (Figure 2) makes further predictions about speciation within the radiation. For example, I found much stronger selection against hybrids resembling the scale-eater phenotype than against against hybrids resembling the hard-shelled prey specialist phenotype. This indicates that a very large fitness valley separates the specialist niche of scale-eating from the ancestral niche of generalist algivore. In contrast, a small fitness valley separates the specialist niche of hard-shelled prey crushing from the ancestral niche of generalist algivore.

Figure 2. Complex snapshot of natural selection on San Salvador Island, Bahamas. Fitness landscape for survival estimated from the survival of F2 hybrids of all three pupfish species placed in a 12-foot field enclosure for 3 months. For reference, photographs show the phenotypes and position of the three parental species on the landscape: generalist, durophage, and scale-eater. Although I found no evidence of a fitness peak corresponding to scale-eaters, there is still strong evidence of a large fitness valley in this region of the morphospace.

These different-sized fitness valleys on the adaptive landscape predict that gene flow between scale-eaters and generalists should be much lower than between hard-shelled prey specialists and generalists. I tested this prediction in my new paper in Molecular Ecology. In my first foray into next-gen sequencing, I used double-digest RADseq (specifically, the Elshire et al. 2011 genotyping by sequencing protocol) to genotype over 13,000 SNP’s in all three species of pupfishes on San Salvador from seven different lakes where at least two species coexist. Fortunately for me, my collaborator Laura Feinstein, a grad student in Ecology at UC Davis, already had this protocol up and running and showed me the ropes. Our study of genetic differentiation supported predictions from the empirical adaptive landscape. I’ll quickly summarize and speculate about our results below.

1. Specializing on scales drives speciation faster than specializing on snails

Across all lakes surveyed, scale-eaters were more genetically differentiated than hard-shelled prey specialists within the same habitat, despite ongoing gene flow in both species. This pattern can be understood with knowledge of the underlying fitness landscape: stronger selection against scale-eater hybrids provides a greater barrier to gene flow than moderate selection against hard-shelled prey specialist hybrids. Furthermore, this pattern of genetic differentiation was consistent across many lakes on the island and many rare dispersal events of these specialist species, suggesting that it is driven by a consistent selective regime, rather than different histories of the two species. Although speciation in these two species is far from complete, the pattern so far suggests that these two very different foraging strategies are driving different rates of speciation.

2. Not all adaptation is the same

We often talk about adaptation in general such as understanding the genetic basis of adaptation or the role of adaptation in driving reproductive isolation. Instead, our results emphasize that the niche matters: not all adaptation is the same. Adapting to a “closer” niche on the adaptive landscape results in less selection against hybrids than adapting to a “distant” niche on the adaptive landscape. This difference in the strength of postzygotic extrinsic isolating barriers – perhaps the very first isolating barrier in this system – may drive different rates of incipient speciation between diverging ecotypes, even within the same habitat. Both specialist pupfish species are rapidly adapting to new resources in a new environment, but the specific performance demands of these very different resources affect the pace of speciation.

3. The niche shapes the topography of the adaptive landscape

The difference in the strength of selection against hybrids between these two specialist niches makes sense when we consider their contrasting performance demands. Specializing on hard-shelled prey, such as snails and ostracods, simply requires modifying a simple lever system (the jaws) for higher mechanical advantage. Furthermore, these prey are not evasive and are often consumed by generalists as well. In contrast, successful scale-eating requires high-speed strikes on evasive prey (i.e., other pupfish!). Furthermore, each strike only provides a small nutritional benefit – a mouthful of skin, mucus, and scales – so that each strike must be very efficient. Indeed, all specialized scale-eating fishes are size-limited relative to their prey. This suggests that scale-eating should require a highly specific and specialized phenotype for success, whereas successful snail-eating may require fewer modifications. These different performance demands might create different topographies on the adaptive landscape – larger fitness valleys, higher-dimensional changes, and steeper fitness peaks – that all result in stronger selection against scale-eater hybrids.

4. Reinforced pre-mating isolation may result from alternative niche environments

Preliminary female mate choice trials in the lab and focal observations in the field suggest that scale-eater females show much stronger preferences for conspecific males than hard-shelled prey specialist females. This may reflect reinforced conspecific mate preferences in scale-eater females to avoid the higher costs of hybrid matings.

5. Is the rarity of a niche connected to speciation rate within that niche?

Finally, I’d like to take this opportunity to speculate wildly. Scale-eating is incredibly rare within pupfishes: to put this in context, the nearest species with convergent ecology is separated by 168 million years of evolution (my proposed index for measuring ecological novelty). I speculate that this rarity reflects an underlying distant, hard-to-reach fitness peak for scale-eating on the adaptive landscape. At the same time, a distant fitness peak surrounded by a large fitness valley results in much stronger selection against hybrids if a population is able to reach such a peak. If this association holds more generally, it suggests a positive correlation between the rarity of a niche and the rate of speciation within that niche: distant fitness peaks are hard to adapt to initially (resulting in rare use of the corresponding resource or niche), but if a population does colonize such a niche, it may evolve reproductive isolation much faster due to stronger selection against hybrids and reinforced pre-mating isolation. In other words, perhaps oddball ecological specialists speciate faster? Stay tuned!

Monday, April 7, 2014

Peaks and Valleys in the Genome

(This post is by Marius – I am just putting it up. Andrew.)

Driven by methodological advances, evolutionary biology is currently much concerned with understanding the way selection shapes the genome. In the search for such signatures of selection – and ultimately the loci associated with them – we often pursue a similar strategy: we compare populations at thousands of genetic markers with the hope of finding genomic regions of particularly high or low differentiation relative to the genome-wide baseline. We then believe that such regions can be directly linked to distinct selective processes. On the one hand, genomic regions of high divergence are thought to be the result of selection acting in opposite ways (divergent selection) between populations. Low divergence regions, on the other hand, are commonly taken as evidence for balancing selection. The results of our recent paper published in Molecular Ecology, however, challenge these common assumptions.

Figure 1. Parallel adaptation to similar derived habitats (blue) from a common source population inhabiting an ecologically distinct habitat (gray).
For our paper, we first implemented theoretical models in which we considered several populations deriving from a common source population into selectively new and similar habitats – that is, parallel adaptation (Figure 1). We demonstrate that among derived populations, this process drives a region of particularly low divergence around a selected locus. How come? Due to common ancestry, the derived populations do not only share the actual variant being selected, but also the genomic background linked to that variant. Thus, the same variant together with this background are driven to fixation in the derived populations. Consequently, when we compare such populations, we find a genomic region of low divergence surrounding a locus involved in parallel adaptation (Figure 2). Admittedly, this explanation for low divergence within parts of a genome is intuitive. Nevertheless, it is normally overlooked when interpreting low divergence regions in genome scans. From now on, let us call such a region a ‘divergence valley’.

Figure 2. The peak-valley-peak divergence signature of parallel adaptation from shared genetic variation. Important to note here is that the selected locus is actually located at the bottom of the divergence valley, and not at any of the flanking peaks!
 To either side of the divergence valley, our models reveal exaggerated divergence (Figure 2). This is because the selected variant and its linked genomic background are associated with different haplotypes in the different derived populations. Such haplotypes then become, to some extent, selected along with the actual variant and its immediately linked background under selection (this process is called ‘genetic hitchhiking’). As a consequence, different haplotypes increase in the different populations to different frequencies. It is important to note here that this phase of genetic hitchhiking only initiates the high-divergence regions flanking the divergence valley! These regions of high divergence – I will refer to them as ‘twin peaks’ from now on – grow higher and become sharper over time, even after selection has fixed the favorable variant at the locus under selection in all derived populations (Figure 2). The reason for this is that the locus under divergent selection between the source and derived populations and under parallel selection among the derived populations acts as a barrier to ongoing gene flow from the source to the derived populations. The divergence valley will thus, to a great extent, be sheltered from such genetic introgression and remain a low-divergence region among derived populations within the genome. Next to it, however, some genetic variation will introgress from migrants stemming from the source population. Because this happens only occasionally and randomly, the through hitchhiking initiated divergence twin peaks grow higher. Also, the twin peaks become sharper over time because even further away from the selected locus, genetic variation can flow almost unconstrained between the source and derived populations. This gene flow homogenizes the genome of the derived to baseline divergence. A detailed explanation and a graphical illustration of these different – yet together acting – processes can be found in our paper. Also, you will find there a thorough dissection of many factors influencing these divergence patterns (recombination rate, strength of selection, time, migration, number of initial colonizers, and multiple interacting selected loci). What I can tell you already is that the above-explained patterns emerged very consistently in all our simulations!

Picture 1: Top: The Sayward River estuary, where one of the marine stickleback samples was taken for our empirical analysis. Bottom: A typical marine stickleback. Note its characteristic armor plating all along the body axis, which is absent in most freshwater stickleback (Picture: M. Roesti).
Agreed, up to now, this blog post has been quite theoretical. Luckily, we have a great model system at hand to take these theoretical predictions out into the wild. That model system is the threespine stickleback fish. Stickleback have repeatedly colonized and adapted to freshwater (parallel adaptation) from a common marine source population since the last glaciation period. This corresponds exactly to our modeled situation above. In a second part of our paper, we thus predicted to find a divergence valley flanked by twin peaks (together, we can refer to them as ‘peak-valley-peak’; Figure 2) around three particular genes. These genes are great candidates for being under strong divergent marine-freshwater selection, and thus seemed ideal to test whether we would find the peak-valley-peak divergence signature of parallel adaptation to freshwater. We included a total of eight freshwater populations from Vancouver Island (BC, Canada) and two marine samples from the coast of that island in our empirical analyses (Picture 1 and 2). As expected, marine and freshwater stickleback proved strongly differentiated at all three genes. To calculate differentiation, we used haplotype information taken from targeted sequencing as well as the classic divergence measure FST calculated at thousands of polymorphisms along the genome (RAD sequencing data). We further applied an alternative approach to calculate differentiation, for which we looked at the separation of marine and freshwater stickleback within many phylogenetic trees along the genome. Now, our main interest was in divergence among the derived populations adapted in parallel to freshwater. Excitingly, comparing these freshwater populations among each other indeed revealed the predicted peak-valley-peak divergence signature around all three genes! As this worked out so well, we then searched the entire stickleback genome for further such signatures and found many more of them. This allowed us to propose new genes that have been important for replicate freshwater adaptation. Interestingly, we also found that those chromosomes harboring many of these signatures of selection exhibited the strongest overall divergence between marine and freshwater stickleback. This indicates that divergently selected loci can drive heterogeneity in genomic divergence on a chromosome-wide scale.

Picture 2: One of many breathtaking watersheds on Vancouver Island (BC, Canada) inhabited by freshwater stickleback (Picture: M. Roesti).
So what does this all mean? Our results show that parallel adaptation – the very process involving similar selection pressures – can drive high population divergence within parts of a genome. These high-divergence regions, however, are not holding the actual targets of selection themselves; instead, these targets are located in particularly low-divergence regions when the same genetic variation has been re-used for adaptation. Our results are certainly relevant to many organisms for which we have evidence or a strong feeling that parallel adaptation from shared variation has happened. Also, the case where similar selection pressures act in different populations on parts of the genome may be more common than what appears ‘ecologically intuitive’ to us. Threespine stickleback fish provide a particularly neat model system because we can here draw on many independent and parallel adaptation events to freshwater. Also, we can sample marine stickleback, contemporary representatives of the genetic source underlying this parallelism.

Overall, our findings should be taken into consideration when reasoning on divergence signatures within a genome. Finally, our insights can be used as explicit tools in the hunt for selection signatures, and ultimately, adaptation genes. I hope you will enjoy reading our paper!

Full story:

Roesti M, Gavrilets S, Hendry AP, Salzburger W, Berner D (2014). The genomic signature of parallel adaptation from shared genetic variation. Molecular Ecology (From the Cover).

Friday, April 4, 2014

The Coelacanth has had its day

Who hasn’t wanted to bring an extinct species back into existence? Sure, there are risks, both physical (T. rex and pathogens) and ethical (Neanderthals), and sure, we’re better off without some species (smallpox and mososaurs), but how about the gastric brooding frog and the thylacine and the dodo and so on? Surely the world would be a better – or at least not worse – place if we hadn’t lost them. Enter the de-extinction movement, which seeks to bring extinct critters back to life. It hasn’t happened yet, of course, and it might never happen given not only the risks but the costs and difficulties. Even better than de-extinction – and without any of the ethical baggage – is when things thought to be extinct are found not to be (unextinction?).

Being a fish guy, one of the most inspiring unextinction stories is the discovery of the coelacanth – though to be extinct for more than 60 million years. Found on December 22, 1938, in the bottom of a pile of fish on a trawling ship by the young curator (Marjorie Courtenay-Latimer) of a tiny museum in East London, South Africa, this first specimen was bundled into a cab with the help of a very reluctant cab driver, sketched iconically and the sketch mailed to Professor J.L.B. Smith at nearby Rhodes University. The discovery rocked the scientific world but was less than ideal given the lack of preservative available in East London. Then came the search for another specimen, found only 14 years later in the Comoros. Here the story only gets better, with midnight calls to the Prime Minister of South Africa, a clandestine military evacuation, and an indignant French establishment. And then, in 1998, a second coelacanth species was found in Indonesia in a fish market by a couple on their honeymoon. This one was quickly named by French scientists who hadn’t seen it, in apparent retaliation for the loss of the Comoros specimen. (If these tidbits intrigue you, read the full coelocanth story in A Fish Caught in Time.)

Marjorie Courtenay Latimer and the famous sketch that started it all.
De-extinction the way it should be – unextinction! This story had always been one of my favorites and so I had long been excited to see a coelacanth – if only in a big vat of preservative. However, few coelacanths are in North American museums, partly because of the monopoly the French exerted for years after the Comoros scoop by the Brits. So I didn’t get to see one until I went to France, where every Podunk museum and aquarium in every tiny town seems to have one – I saw mine in Biarritz. My daughter even got to see it, although I am not sure at the age of one she had much appreciation for its scientific significance. Truly an inspiring moment – although some day I would love to see one in the wild (probably harder to see than nearly anything else).

The Biarritz coelacanth - a treat for me and for Aspen!
Of course, coelacanths remain very rare, perhaps forever at risk of re-extinction, something we should surely seek to prevent. Indeed, the goal of preserving truly unique species is gaining steam in conservation biology. The basic idea is that many species are likely at risk of extinction and we need some sort of criterion for deciding which to preserve. One criterion that has been put forth is phylogenetic distinctiveness. That is, the species that warrant the most protection are those that represent the last remaining bits of long isolated branches of the evolutionary tree – lose that last species and forever lose a big chunk of the history of life. A recent incarnation of this idea is EDGE (evolutionarily distinct globally endangered), which seeks to prioritize species conservation based on a joint consideration of phylogenetic distinctiveness and degree of endangerment. So far so good; finally conservation biologists are fully using evolutionary criteria for species conservation! Something all evolutionary biologists can get behind – or is it?

A few weeks ago, I was in College Station, at Texas A&M University, as one of the invited speakers for the Ecological Integration Symposium organized by graduate students (my host was Emily Rose). My talk was on ecological speciation, David Reznick spoke on eco-evolutionary dynamics, Brian Bowen discussed marine speciation, and Tom Lovejoy gave an overview of global climate change effects. At the end of our plenary session, we had a panel discussion. At first, the four of us thought it might be awkward as our talks had been on very different things – but we quickly converged on a topic to which we could all provide perspectives: What, precisely, should we be conserving? A large part of the discussion focused on the importance of preserving not only species but also intra-specific variation, but we also discussed which species should be preserved. At one point, I went through the above rationale about phylogenetic distinctiveness being an important criterion and then Brian grabbed the mic out of my hand.

“THE COELACANTH HAS HAD ITS DAY” was the first sentence out of his mouth. He then went on to describe how species come and go all the time and those old rare relicts just hanging on (coelacanths, tuataras) are probably not long for this world (extinctive?) regardless of human influence – so perhaps we shouldn’t bother. Instead, we should focus our efforts on groups that are rapidly diversifying – African cichlids was his prime example – as they are the future of biodiversity. Ok, sure, I like cichlids as much as (probably more than) the average person, but let the coelacanth go? Heresy. Fear. Fire. Foes. Right then and there I excommunicated him from the pantheon of evolutionary biologists, revoked his citizenship in a compassionate humanity, unfriended him on Facebook, and started a smear campaign to discredit him.

Me and Brian Bowen, the most dangerous man alive - for coelacanths anyway. (Photo by Melissa Giresi.)
On sober (actually just the opposite) subsequent refection, however, I began to question my reaction. Try this thought experiment. How many cichlid species is the coelacanth worth? I think we can surely say at least one. Taking inspiration from Phil Pister’s “species in a bucket”, if I had all of the world’s Pseudocrenilabrus multicolor in a bucket in my left hand and all the world’s coelacanths in a bucket in my right hand, I would probably saw through my left wrist before dropping the bucket in my right. (I might hesitate longer if the hands were reversed.) I would probably decide the same for 10 cichlids or maybe a hundred but what about a thousand or ten thousand – what if it was the entire cichlid fauna of Lake Tanganika or Malawi or Victoria? By the EDGE perspective, I expect that I would save the coelacanth. By the de-extinction perspective, I would probably do the same (it would be much harder to re-evolve the coelacanth than start a new radiation of cichlids – after all, they do it all over the place). But by the Bowen perspective, I would clearly drop the coelacanth without a second thought. And at some level, I see the point. Coelacanths aren’t going to give us anything new. At best, they will still be around a million years in the future looking pretty much the same. The cichlids, however, will likely produce many new species in that time. The future of biodiversity is perhaps better off with the cichlids than coelacanths.

Fortunately, I am not a manager and don’t have to make such decisions, because the truth is I want both cichlids and coelacanths! But perhaps I could do without ticks and chiggers and dengue and AIDS and TB and definitely poison ivy.

An amazing giant isopod in the Texas A and M invertebrate collection. (Photo by Melissa Giresi.)

Tuesday, April 1, 2014

Carnival #70 is up!

Carnival of Evolution #70 is now up!  We had an embarrassment of riches this month, with guest posts from Jacques Labonne about the new Basque fish blog, Fish&Bits, Dan Hasselman on how Anthropogenic habitat disturbance can impact species integrity, Katja Räsänen on the mosaic of reproductive isolation… not to mention posts from Andrew on the meaning of “extinctive” and his visit to Darwin’s pub.

In the end, though, we nominated a fascinating post from Jonathan Richardson about microgeographic adaptation and the spatial scale of evolution.  If you've ever wondered just how “local” local adaptation is, this post will give you some food for thought.

By the way, it’s great to be getting so many guest posts, and we’d like to encourage more.  If you’re a researcher in evolutionary ecology or eco-evolutionary dynamics and you’d like to contribute, please feel free to send an email to Andrew Hendry!

The theme of the new Carnival, at Synthetic Daisies, is evolutionary games.  Enjoy.

Fig. 1.  Evolutionary game theory.  I used to own a stand-up Millipede console.  Now that was a great video game; I wish I still owned it.  Galaga, Defender, Millipede, Donkey Kong, Tempest, Q*bert, Marble Madness… those were the days.